Passive Integrated Transponder Tags: Review of Studies on Warmwater Fishes with Notes on Additional Species

Articles Passive Integrated Transponder Tags: Review of Studies on Warmwater Fishes With Notes on Additional Species

W. Chris Musselman, Thomas A. Worthington, Joshua Mouser, Desiree M. Williams, Shannon K. Brewer*

W.C. Musselman, T.A. Worthington, J. Mouser, D.M. Williams Oklahoma Cooperative Fish and Wildlife Research Unit, 007 Agriculture Hall, Oklahoma State University, Stillwater, Oklahoma 74078

S.K. Brewer U.S. Geological Survey, Oklahoma Cooperative Fish and Wildlife Research Unit, 007 Agriculture Hall, Oklahoma State University, Stillwater, Oklahoma 74078-3051

Abstract Although numerous studies have assessed retention and survival of passive integrated transponder (PIT) tags, data are scattered and information gaps remain for many diminutive fishes. Our study objectives were to 1) systematically review PIT tag studies and summarize retention, growth, and survival data for warmwater fishes; and 2) conduct a laboratory study to evaluate the retention, survival, and growth effects of intracoelomic-placed, half duplex PIT tags on six small-bodied species common to warmwater streams. Our systematic review suggested small sample sizes were common within PIT tag retention and survival studies (39% with n 20) and that many experiments (15%, 14 of 97) failed to use control fish as part of their evaluations. Studies focused primarily on short-term changes (15 d to 2 y) in tag retention and survival. Tag retention was equal to or greater than 90% in 85% of the experiments reviewed and median survival was 92%. Growth was reported by fishes in the majority of reviewed studies. We found similar results after PIT tagging (peritoneum tagging using 12- or 23-mm half duplex tags) adult Cardinal Shiner Luxilus cardinalis, Central Stoneroller Campostoma annomalum, Greenside Darter Etheostoma blennioides, Orangethroat Darter Etheostoma spectabile, Slender Madtom Noturus exilis, and juvenile Smallmouth Bass Micropterus dolomieu. Tag retention for all species was high, with only one tag loss recorded after 60 d. Survival was also high (88%) for all of our species with the exception of Orangethroat Darter (56% survival). No significant difference in mean growth between treatment and control groups was found. Both our results and the findings of the literature review suggested generally high tag retention and low mortality in tagged fishes (across 31 species reviewed). However, within our study (e.g., Orangethroat Darter) and from the literature, examples of negative effects of PIT tagging on fishes were apparent, suggesting methodological testing is prudent before using PIT tags in field studies. We suggest future studies would benefit from addressing the behavioral implications that may be associated with tagging and examination of longer-term tag retention. Furthermore, standard reporting (i.e., sample sizes) in PIT tag studies would be beneficial, and use of control subjects or groups for statistical comparisons is needed.

Keywords: survival; tagging; retention Received: December 6, 2016; Accepted: May 10, 2017; Published Online Early: June 2017; Published: December 2017 Citation: Musselman WC, Worthington TA, Mouser J, Williams DM, Brewer SK. 2017. Passive integrated transponder tags: Review of studies on warmwater fishes with notes on additional species. Journal of Fish and Wildlife Management 8(2):353-364; e1944-687X. doi:10.3996/122016-JFWM-091 Copyright: All material appearing in the Journal of Fish and Wildlife Management is in the public domain and may be reproduced or copied without permission unless specifically noted with the copyright symbol &. Citation of the source, as given above, is requested. The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service. * Corresponding author: [email protected]

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Introduction in our study were consistent across other warmwater fishes. We also report patterns across studies to provide As smaller passive integrated transponder (PIT) tags recommendations for future PIT tag studies. have become available with technological advances, their use has increased in many studies in which Methods individual identification is needed. Passive integrated transponder tags are glass-encapsulated microchips Literature review with unique identification, long operating time, and To provide an indication of the state of knowledge in passive detection—characteristics that have increased relation to survival and retention of PIT tags in the accuracy of mark–recapture estimates (Gibbons and Andrews 2004; Hewitt et al. 2010) and their application nonsalmonid fishes, we conducted a literature search to an array of study objectives. Recaptures of PIT- by using ISI Web of Science in 2015. Four search strings tagged fishes have been used to estimate population were used, which were formed using the combinations size (Pine et al. 2003), growth (Walters et al. 2012), of the following keywords: ‘fish’ AND ‘passive-integrat- survival (Hewitt et al. 2010), movement (Skalski and ed-transponder’ OR ‘PIT Tag’ AND ‘retention’ OR Gilliam 2000), habitat use (Teixeira and Cortes 2007), ‘survival’. Within Web of Science, search results were predation (Ryan et al. 2003), behavior (McCormick and screened based on the titles and abstracts and studies Smith 2004), and sampling efficiency (Price and on salmonids, marine, and estuarine species and non- Peterson 2010). fish species (e.g., crayfish, salamanders) were omitted. Small tags (9–12 mm) implanted into the body cavity The resulting literature was accessed and further (intracoelomic) have made PIT tags an effective option filtered to remove studies that provided no information for studying small-bodied fishes (e.g., Dixon and Mesa on survival or retention or were focused on anguilliform 2011), but fish size remains a limiting factor (Prentice et species. al. 1990a; Lucas and Baras 2000; Skalski et al. 2009). Once the final set of literature was gathered, each Below a certain size, individuals may have slower growth and higher mortality after intracoelomic PIT tag injection paper was examined for general information: the year of (Prentice et al. 1990a). In addition, PIT tag retention is publication, journal, taxonomic group studied, and size dependent (Acolas et al. 2007), and the size objectives. For each paper, the number and identity of threshold is associated with loss of fitness (i.e., reduced the species studied and the taxonomic family were growth and survival), and unacceptable levels of tag recorded. The study objectives in relation to the use of retention are species specific (McCormick and Smith PIT tags were categorized into seven groups, with 2004; Jepsen et al. 2005). Although these relationships studies sometimes belonging to multiple categories: 1) have been generally well established in the literature for tag retention, 2) fish survival, 3) fish growth, 4) behavioral salmonids (Skalski et al. 2009; Cooke et al. 2011), responses, 5) different PIT tagging methodologies, 6) information is lacking for many warmwater fishes (Cooke different anatomical tagging locations, and 7) compar- et al. 2011). isons with other fish-marking procedures. Tag loss and tagging effects on growth and survival Within each individual study, more than one experi- violate mark–recapture assumptions and bias parameter ment was often identified, and was eventually used to estimates that can handicap attempts to effectively manage populations (Burnham et al. 1987). Bolland et al. summarize retention and survival for each species. For (2009) recommended retention and survival be evaluat- our analysis, we split studies into experiments if they ed for each species before field studies. This is especially used different species, different methodologies (e.g., tag important for juveniles and other small-bodied fishes size, tagging location, tagging method, PIT tags com- where the risk of negative tag effects are increased bined with other types of tags), different sizes of fish, (Prentice et al. 1990a). Although numerous studies have different times, or different study locations (e.g., labora- assessed PIT tag retention and survival, data are tory, fish pond, or field). If PIT tags were implanted in scattered and information gaps remain for fishes in multiple locations on the same fish, each anatomical certain ecosystems (e.g., warmwater streams; Cooke et al. location was deemed an experiment. For each experi- 2011). Therefore, the study objectives were to 1) ment, data were recorded on the study duration, systematically review PIT tag studies and summarize location type, source of the fish (wild or hatchery), and retention and growth and survival data for nonsalmonid sample size. The tag size (length and width), tagging fishes; and 2) conduct a laboratory study to evaluate the method, and tagging location were also recorded. Where retention, survival, and growth effects of intracoelomic available, statistics on percentage of tag retention, fish PIT tags on six small-bodied species common to warmwater streams. Our laboratory study was conducted to survival and growth (positive or negative), and whether it ensure retention and survival were appropriate to follow was statistically different from a control group were up with a field-based study evaluating movement of collated. If a study had multiple experiments using a select small-bodied fishes. Because our laboratory single species, we recorded these separately. If retention, experiment was limited by sample size, we placed our survival, or growth statistics were reported at multiple experiments into context by comparing them with data time steps through an experiment, information from the from the literature to see whether the patterns observed last time step was used.

Journal of Fish and Wildlife Management | www.fwspubs.org December 2017 | Volume 8 | Issue 2 | 354 PIT Tag Retention and Survival W.C. Musselman et al.

Table 1. Characteristics of six warmwater fish species that were collected from Flint Creek, OK in 2012 to determine passive integrated transponder (PIT) tag retention in the laboratory. All fish were tagged in the peritoneum with 12- or 23-mm (tag size) half duplex PIT tags. The number of individuals (N) varied by each species due to availability at sample locations. The mean initial total length (TL) and mean initial weight (WT) are provided for each study species. Variance was reported as SD.

Common name Scientific name N TL 6 SD (mm) WT 6 SD (g) Tag size (mm) Cardinal Shiner Luxilus cardinalis 24 91.1 6 9.6 6.8 6 2.3 12.0 3 2.12 Central Stoneroller Campostoma annomalum 16 94.3 6 18.2 7.3 6 4.5 12.0 3 2.12 Slender Madtom Noturus exilis 26 76.8 6 10.0 3.4 6 1.4 12.0 3 2.12 Orangethroat Darter Etheostoma spectabile 18 60.2 6 5.7 2.1 6 0.7 12.0 3 2.12 Greenside Darter Etheostoma blennioides 6 94.8 6 9.3 6.5 6 1.7 12.0 3 2.12 Smallmouth Bass Micropterus dolomieu 50 148.0 6 10.8 31.0 6 7.2 23.0 3 3.65

Laboratory trials Controlfishesweresubjecttothesamehandlingas Laboratory experiments were conducted on six warm- treatment fishes (i.e., anesthetized, measured, water fishes in 2012 to assess tag retention and the weighed), but were not tagged. The same person effects on fish growth by intracoelomic PIT tagging. Wild (W.C.M.) conducted all tagging. fishes included in the laboratory study were Cardinal Tags were injected using a 12-gauge hypodermic Shiner Luxilus cardinalis (n ¼ 24), Central Stoneroller needle (12-mm tag) or surgically implanted using a Campostoma annomalum (n ¼ 16), Greenside Darter scalpel and manual insertion (23-mm tag) into the Etheostoma blennioides (n ¼ 6), Orangethroat Darter peritoneum from underneath the pectoral fin following Etheostoma spectabile (n ¼ 18), and Slender Madtom methods of Prentice et al. (1990b). Smaller species (e.g., Noturus exilis (n ¼ 26; Table 1). Wild fishes were collected minnows, darters, and madtoms) were placed in an from Flint Creek, a third-order tributary of the Illinois individual 38-L aquarium with a control fish of the same River located in northeast Oklahoma by using standard species. Smallmouth Bass were placed into three seining methods (Bonar et al. 2009). Water temperatures replicate 2,400-L tanks in groups of ten (control n ¼ 5, at the time of fish collections ranged from 21 to 248C. treatment n ¼ 5). These holding densities were within the Juvenile Smallmouth Bass Micropterus dolomieu (n ¼ 50), range found under field conditions (S.K. Brewer, unpub- acquired from the Kansas Department of Wildlife and lished data). Parks (Pratt Fish Hatchery, Pratt, KS), were also included Experiments lasted a minimum of 30 d. Fish were then in the study (Table 1). All fishes were acclimated to removed from the tanks, anesthetized, measured (total laboratory conditions for a minimum of 2 wk and placed length), weighed, and scanned with a hand-held PIT tag on a twice-daily feeding schedule with weekly water reader (DataTracer, Oregon RFID) for the presence of the changes and daily water-quality monitoring (i.e., pH, tag. Treatment fishes that retained tags after 30 d were dissolved oxygen, ammonia, and temperature). Water held for an additional 30 d, but they were placed in temperatures in the laboratory were 23–258C during the larger 2,400-L tanks. Treatment Smallmouth Bass were study. Dissolved oxygen and ammonia were maintained still kept in separate 2,400-L tanks to avoid predation on at acceptable levels and the pH was 6.8–8.2. All fishes smaller study species. At the end of the experiments, fish were fed a dense-culture feed or freeze-dried krill were euthanized using a lethal dose of MS-222, (Aquatic Ecosystems, Apopka, FL). measured, weighed, and then preserved in 10% formalin. Fish were haphazardly assigned to a treatment or Growth rates (final weight initial weight), survival control group. Before handling, all fish were anesthe- (percentage alive after the trial), and tag retention tized using tricaine methanesulfonate (MS-222; ap- (percentage retaining tags after the trial) were calculated proximately 2.5 mL/L stock solution of 20 g of MS-222 at the conclusion of the experiment. Significant differ- and 50 g of NaHCO3/L, Hauer and Lamberti 2006). ences (a ¼ 0.05) in mean growth for treatment vs. control Upon loss of equilibrium, fish were measured to the fish by species were assessed using a Welch’s t-test in R nearest 1.0 mm (total length) and weighed to the (R Core Team 2012). Welch’s t-test does not make the nearest 0.1 g. All treatment fishes, except Smallmouth assumption of homogeneity of variance and uses a Bass, were tagged with a 12-mm half duplex PIT tag correction to adjust degrees of freedom (Field et al. (OregonRFID,Portland,OR).Halfduplextagswere 2012). Normality of growth data by species and chosen over full duplex tags because they are less treatment were evaluated using a Shapiro–Wilk test. susceptible to noise (i.e., interference), and 12 mm is the smallest tag size currently produced. Because of Results their larger size, Smallmouth Bass were tagged with a 23-mm half duplex PIT tag (Oregon RFID). Larger tag Literature review size is associated with greater read range and is The literature search returned 167 individual articles of advantageous in field studies (see description at which 29 met the review criteria (e.g., retention and https://www.oregonrfid.com/index.php?main_page¼ survival) of PIT tag studies on non-salmonid fishes. page&id¼31&zenid¼bk2kfb9p1c1mev066aappu07h5). Publication dates ranged from 1989 to 2015, with a

Journal of Fish and Wildlife Management | www.fwspubs.org December 2017 | Volume 8 | Issue 2 | 355 PIT Tag Retention and Survival W.C. Musselman et al.

general increase in publications since 2009. There was a papers each. The least common methods reported were clear bias in the journals where studies were published, injection into the isthmus and esophageal implants, with with only nine outlets represented. More than half (15 of one paper each. 29) of the studies were published in the North American We identified several experiments, which were used to Journal of Fisheries Management. Additional journals summarize tag retention and fish survival by species. represented were the Journal of Applied Ichthyology (n Statistics on tag retention and fish survival were available ¼ 3), Ecology of Freshwater Fish (n ¼ 2), Transactions of the from the majority of the experiments (Table 2). Across all American Fisheries Society (n ¼ 2), North American Journal experiments, retention ranged from 13 to 100%. Tag of Aquaculture (n ¼ 2), Progressive Fish-Culturist (n ¼ 2), retention was equal to or greater than 90% in 85% of and three other journals with one publication each. experiments. Fish survival was more variable, although Studies were biased toward those carried out in the survival was equal to or greater than 90% in 57% of United States (72%; including one field study in Lake Erie, experiments, ranging between 0 and 100% (median ¼ United States and Canada). Three studies were conduct- 92%). Control groups were used in 83 of 97 experiments, ed in the UK; two in Belgium; and one each in Canada, allowing significant differences in survival to be calcu- Germany, and Japan. The majority of studies focused on lated for some studies (Table 2). Twenty-six of the a single species (n ¼ 25), with one study containing control-paired experiments did not report statistics information on two species and three studies comparing relating survival between treatment groups. For the three species. Information was reviewed on 31 species remaining experiments, there was no difference in with Muskellunge Esox masquinongy (n ¼ 4), Largemouth survival for the majority (n ¼ 41); however, significantly Bass Micropterus salmoides (n ¼ 2), and Burbot Lota lota lower survival was reported for the treatment group on (n ¼ 2) represented in multiple studies. The 31 species sixteen occasions. Of the 47 experiments where growth represented 15 families, with most species belonging to data were available, growth was reported in all but one five families: Cyprindae (26%), Cottidae (10%), Ictaluridae instance. Lastly, sample sizes varied greatly across (10%), and Lepisosteidae (10%). experiments with 39% (38 of 97) of studies using 20 or The papers covered multiple objectives, but those fewer individuals. objectives were not equally represented. As expected given the search terms, after tag retention, fish survival Laboratory trials was the most common study area (83% of studies; Table The mean total length of the experimental fishes 2). Information on fish growth in relation to tagging was (Table 3; Tables S1 and S2, Supplemental Material) ranged reported in almost half the studies (n ¼ 12), whereas from 60 mm for Orangethroat Darter to 148 mm for studies comparing PIT tags to other tagging methods juvenile Smallmouth Bass. All species growth data fit the were also well represented (41% of studies). Nine studies assumption of normality. Survival 24 h post tagging was compared different anatomical tagging locations, where- 100% for all species and remained high for the study as different insertion methods (e.g., injecting vs. inci- duration (Table S3, Supplemental Material). After 30 days, sions) were the subject of four papers. Studies reporting treatment survival was 100% for Cardinal Shiner, Central Stoneroller, Greenside Darter, and Slender Madtom, with information on fish behavior focused on swimming a single mortality for each of Smallmouth Bass and performance (n ¼ 2), feeding (n ¼ 2), and net avoidance Orangethroat Darter (Table 3). After 60 d, there was a (n ¼ 1). single Central Stoneroller mortality and three additional Studies also varied in the location where they were Orangethroat Darter mortalities. Survival remained con- conducted, the study duration, and the sample size. A stant for all other species (Table 3). Tag retention after 60 majority of the 29 studies was conducted in the d was 100% for all species except Orangethroat Darter. laboratory (n 15), but field (n 4) and aquaculture ¼ ¼ Orangethroat Darter lost a single tag in the first 30 d, pond (n 9) setups were also used. There was also one ¼ reducing retention to 88%, but the overall retention paper that included both lab and pond setups. Study percentage dropped further at 60 d due to mortalities duration was highly variable, ranging from 15 d to more (e.g., four of five fish retained tags; Table 3). There were than 2 y. Wild fish (n ¼ 16) were more commonly used in no significant differences in mean growth between studies compared to hatchery-raised fish (n ¼ 13). The treatment and control groups for all species (Figure 1). number of fish tagged per experiment ranged from 4 to 930 individuals (median ¼ 32). Tagging methodology was mainly split between tags Discussion implanted into the peritoneal or dorsal musculature by The use of PIT tags in the conservation and using injection, or into the peritoneal by incision. The management of fish species is a valuable tool; however, most common methods and locations reported were PIT understanding tagging limitations (i.e., changes to fish tags inserted via incision into the peritoneal cavity and fitness and the likelihood of tag retention) is critical. For injected into the dorsal musculature (41% of studies all our study species, we observed high PIT tag retention, each). Other well-represented methods were injection with only a single Orangethroat Darter losing a tag. This into the peritoneal cavity (n ¼ 11). Injection into the is consistent with the findings of the review in which cheek musculature and operculum were reported in two reported retention across the experiments was high. Our

Journal of Fish and Wildlife Management | www.fwspubs.org December 2017 | Volume 8 | Issue 2 | 356 Table 2. Summary of reviewed passive integrated transponder (PIT) tag studies on warmwater fishes resulting from a literature search by using ISI Web of Science in 2015. Four Survival and Retention Tag PIT search strings were used: ‘fish’ AND ‘passive-integrated-transport’ OR ‘PIT Tag’ AND ‘retention’ OR ‘survival’. Within Web of Science, search results were screened based on the titles ora fFs n idieMngmn w.wpb.r eebr21 oue8|Ise2|357 | 2 Issue | 8 Volume | 2017 December www.fwspubs.org | Management Wildlife and Fish of Journal and abstract and studies on salmonids, marine and estuarine species and nonfish species (e.g., crayfish and salamanders) were omitted. The resulting literature summarized included percentage of tags retained (R) by fish at the study endpoint, survival (S), and growth (G). Stage of each species is reported as indicated by the reviewed manuscript (source) as J ¼ juvenile or A ¼ adult. ‘‘Other’’ refers to criteria unique to specific experiments: weight classes, size classes in fork length (FL) or total length (TL), different tagging locations, temporal differences, and additional tag differences. N refers to the number of fish used in the trials and length indicates the study duration. When possible, we calculated percentage of retention of fish holding tags. In some cases, investigators estimated retention (%) and we report that below. We report growth direction as positive (þ)or negative () as studies used different approaches to estimate growth. ‘‘Method’’ refers to tagging method: 1 ¼ insertion or 2 ¼ injection. Locations of tag are as follows: 1 ¼ peritoneal cavity; 2 ¼ dorsal musculature; 3 ¼ cheek musculature; 4 ¼ opercular; 5 ¼ esophageal implant; 6 ¼ isthmus. Type refers to the environment where the study took place: 1 ¼ lab; 2 ¼ pond; 3 ¼ field. Species included in the review were Alewife Alosa pseudoharengus, Alligator Gar Atractosteus spatula, White Sucker Catostomus commersonii, Mottled Sculpin Cottus bairdii, Shorthead Sculpin C. confusus, Bullhead Cottus gobio, Moapa White River Springfish Crenichthys baileyi moapae, Lost River Sucker Deltistes luxatus, Northern Pike Esox Lucius, Muskellunge Esox masquinongy, Humpback Chub Gila cypha, Rio Grande Silvery Minnow Hybognathus amarus, Blue Catfish Ictalurus furcatus, Channel Catfish Ictalurus punctatus, Spotted Gar Lepisosteus oculatus, Longnose Gar Lepisosteus, Pumpkinseed Lepomis gibbosus, European Chub Leuciscus cephalus, Common Dace Leuciscus leuciscus, Burbot Lota lota, Largemouth Bass Micropterus salmoides, Oriental Weather Loach Misgurnus anguillicaudatus, Nile Tilapia Oreochromis niloticus, Flathead Chub Platygobio gracilis, Topmouth Gudgeon Pseudorasbora parva, Flathead Catfish Pylodictis olivaris, Common Roach Rutilus rutilus, Walleye Sander vitreus, Pallid Sturgeon Scaphirhyncus albus, Creek Chub Semotilus atromaculatus, European Catfish Silurus glanis.

Tag size Species (mm) Stage Other N Length (d) R (%) G S (%) Method Location Type Source Alosa pseudoharengus 23 3 3.8 A 49 38 100 57 1 1 1 Castro-Santos and Vono 2013 A. pseudoharengus 23 3 3.8 A 49 38 95 41 1 5 1 Castro-Santos and Vono 2013 Atractosteus spatulae 10 800–876 100 2 2 2 Buckmeier and Reeves 2012 Catostomus commersoniib 12.5 19 30 100 32 1 1 1 Ficke et al. 2012 C. commersoniib 23 18 30 100 44 1 1 1 Ficke et al. 2012 Cottus bairdii 12 3 2.1 26 28 96 þ 96 2 1 1 Ruetz et al. 2006 Cottus confusus 12.5 3 2 ,80 mm TL 20 29 100 100 2 1 1 Zaroban and Anglea 2010 C. confusus 12.5 3 2 ,80 mm TL 20 29 12.5 80 2 2 1 Zaroban and Anglea 2010 C. confusus 12.5 3 2 80 mm TL 20 29 90 100 2 1 1 Zaroban and Anglea 2010 C. confusus 12.5 3 2 80 mm TL 20 29 35 100 2 2 1 Zaroban and Anglea 2010 Cottus gobio 12 3 2.1 A 50–64 mm 13 49 100 þ 100 1 1 1 Knaepkens et al. 2007 C. gobio 12 3 2.1 A 65–79 mm 21 49 90 þ 100 1 1 1 Knaepkens et al. 2007 C. gobio 12 3 2.1 A 80–94 mm 10 49 100 þ 90 1 1 1 Knaepkens et al. 2007 Crenichthys baileyi moapae 9 3 2 90 41 100 96 1 1 3 Dixon and Mesa 2011 Deltistes luxatus 12.45 3 2.02 J 51 34 98 90 2 1 1 Burdick 2011 Esox luciusa,b 12 3 2.15 J 71 520 94 þ 25 2 2 2 Huhn¨ et al. 2014 E. luciusa,c 12 3 2.15 J Also tagged with T-bar anchor tag 72 520 100 þ 28 2 2 2 Huhn¨ et al. 2014 E. luciusa,b 12 3 2.15 J Also tagged with opercular tag 70 520 100 þ 31 2 2 2 Huhn¨ et al. 2014 E. luciusa,b 12 3 2.15 J Also tagged with streamer tag 71 520 100 þ 07 2 2 2 Huhn¨ et al. 2014 Esox masquinongy 12.45 A Spider Lake Chain 49 365 88 2 3 3 Jennings et al. 2009 E. masquinongy 12.45 A Mud-Callahan Lake 24 365 95.8 2 3 3 Jennings et al. 2009 E. masquinongya 12 3 2.1 A 841 3,652 .99 2 2 3 Rude et al. 2011 ..Msemne al. et Musselman W.C. E. masquinongy 12 3 2.1 J Illinois 100 153 100 þ 84 2 1 2 Wagner et al. 2007 E. masquinongy 12 3 2.1 J Illinois 100 153 100 þ 87 2 2 2 Wagner et al. 2007 E. masquinongy 12 3 2.1 J Wisconsin 200 210 100 þ 92 2 1 2 Wagner et al. 2007 E. masquinongy 12 3 2.1 J Wisconsin 200 210 99 þ 93 2 2 2 Wagner et al. 2007 E. masquinongy 11.5 3 2.1 J 150 176 100 91 2 2 1 Younk et al. 2010 E. masquinongy 11.5 3 2.1 J 150 176 92 89 2 3 1 Younk et al. 2010 Gila cypha 8.4 J 40–49 mm TL 40 60 100 þ 88 2 1 1 Ward et al. 2015 Table 2. Continued. Survival and Retention Tag PIT

ora fFs n idieMngmn w.wpb.r eebr21 oue8|Ise2|358 | 2 Issue | 8 Volume | 2017 December www.fwspubs.org | Management Wildlife and Fish of Journal Tag size Species (mm) Stage Other N Length (d) R (%) G S (%) Method Location Type Source G. cypha 12.5 J 40–49 mm TL 40 60 88 þ 80 2 1 1 Ward et al. 2015 G. cypha 8.4 J 50–59 mm TL 40 60 81 þ 93 2 1 1 Ward et al. 2015 G. cypha 12.5 J 50–59 mm TL 40 60 97 þ 80 2 1 1 Ward et al. 2015 G. cypha 8.4 J 60–69 mm TL 40 60 100 þ 100 2 1 1 Ward et al. 2015 G. cypha 12.5 J 60–69 mm TL 40 60 92 þ 95 2 1 1 Ward et al. 2015 G. cypha 8.4 J 70–79 mm TL 40 60 98 þ 100 2 1 1 Ward et al. 2015 G. cypha 12.5 J 70–79 mm TL 40 60 95 þ 100 2 1 1 Ward et al. 2015 Hybognathus amarus 12.5 3 2.07 A 80 32 90 þ 87 1 1 1 Archdeacon et al. 2009 H. amarus 12.5 3 2.07 A 80 32 89 þ 50 2 1 1 Archdeacon et al. 2009 H. amarus 12.5 3 2.07 280 49 90 90 1 1 1 Archdeacon et al. 2009 Ictalurus furcatusa 8.5 3 2.1 81 182 100 96 2 2 2 Bodine and Fleming 2014 Ictalurus punctatus 10 3 2.1 A 75 365 97 2 2 2 Moore 1992 I. punctatus 10 3 2.1 A 126 730 97 2 2 2 Moore 1992 Lepisosteus oculatusa 4 800–876 100 2 2 2 Buckmeier and Reeves 2012 Lepisosteus osseusa 16 500–599 100 2 2 2 Buckmeier and Reeves 2012 Lepomis gibbosusb,c 12 3 2 20 21 100 þ 90 1 1 1 Stakenas et al. 2009 Leuciscus cephalus 12 3 2.1 J 87–167 mm FL 80 182 100 98 1 1 1 Bolland et al. 2009 L. cephalus 23 3 3.4 J 114–210 mm FL 101 182 100 98 1 1 1 Bolland et al. 2009 L. cephalusb 23 3 3.4 J 87–167 mm FL 80 182 100 96 1 1 1 Bolland et al. 2009 L. cephalusb 23 3 3.4 J 114–210 mm FL 100 182 100 100 1 1 1 Bolland et al. 2009 Leuciscus leuciscus 12 3 2.1 J 80 182 100 96 1 1 1 Bolland et al. 2009 L. leuciscusb 23 3 3.4 J 80 182 97 73 1 1 1 Bolland et al. 2009 Lota lota 9.0 3 2.03 J 50 365 100 þ 94 2 2 1 Ashton et al. 2014 L. lota 9.0 3 2.03 J 50 365 100 þ 98 2 1 1 Ashton et al. 2014 L. lota 9.0 3 2.03 J 50 365 98 þ 92 1 1 1 Ashton et al. 2014 L. lota 23 A 101 60 100 92 1 1 1 Gardunio and Myrick 2012 Micropterus salmoides 21 3 10 A 22 730 100 91 2 1 3 Harvey and Campbell 1989 M. salmoides 12.34 3 2.04 March 18 365 95 þ 89 2 1 2 Siepker et al. 2012 M. salmoides 12.34 3 2.04 March 20 365 100 þ 85 2 2 2 Siepker et al. 2012 M. salmoidesd 11 3 2.86 March 15 365 100 þ 93 2 1 2 Siepker et al. 2012 M. salmoidesd 11 3 2.86 March 13 365 100 þ 100 2 2 2 Siepker et al. 2012 M. salmoides 12.34 3 2.04 April 32 365 100 þ 97 2 1 2 Siepker et al. 2012 M. salmoides 12.34 3 2.04 April 32 365 100 þ 97 2 2 2 Siepker et al. 2012 M. salmoidesd 11 3 2.86 April 26 365 100 þ 100 2 1 2 Siepker et al. 2012 M. salmoidesd 11 3 2.86 April 32 365 100 þ 100 2 2 2 Siepker et al. 2012 Misgurnus anguillicaudatus 12.05 3 2.07 J 32 30 97 þ 94 2 1 1 Kano et al. 2013 M. anguillicaudatus 12.05 3 2.07 J 32 30 97 þ 97 1 1 1 Kano et al. 2013 Oreochromis niloticusb 10.3 J ,3 g 8 49 100 þ 75 1 1 1 Baras et al. 1999 b O. niloticus 10.3 J 3–4 g 11 49 100 þ 73 1 1 1 Baras et al. 1999 al. et Musselman W.C. O. niloticusb 10.3 J 4–7 g 12 49 100 þ 92 1 1 1 Baras et al. 1999 O. niloticusb 10.3 J 7–15 g 24 49 100 þ 100 1 1 1 Baras et al. 1999 O. niloticus 10.3 J ,3 g 12 49 90 þ 83 1 1 1 Baras et al. 1999 O. niloticus 10.3 J 3–4 g 14 49 90 þ 71 1 1 1 Baras et al. 1999 O. niloticus 10.3 J 4–7 g 7 49 86 þ 100 1 1 1 Baras et al. 1999 O. niloticus 10.3 J 7–15 g 7 49 100 þ 100 1 1 1 Baras et al. 1999 O. niloticus 10.3 J ,3 g 10 49 0 2 1 1 Baras et al. 1999 I a eeto n Survival and Retention Tag PIT ora fFs n idieMngmn w.wpb.r eebr21 oue8|Ise2|359 | 2 Issue | 8 Volume | 2017 December www.fwspubs.org | Management Wildlife and Fish of Journal

Table 2. Continued.

Tag size Species (mm) Stage Other N Length (d) R (%) G S (%) Method Location Type Source O. niloticus 10.3 J 3–4 g 10 49 50 20 2 1 1 Baras et al. 1999 O. niloticus 10.3 J 4–7 g 10 49 100 30 2 1 1 Baras et al. 1999 O. niloticus 10.3 J 7–15 g 10 49 100 50 2 1 1 Baras et al. 1999 O. niloticus 10.3 J 15–20 g 10 49 100 90 2 1 1 Baras et al. 1999 O. niloticus 10.3 J 20–25 g 10 49 100 100 2 1 1 Baras et al. 1999 Platygobio gracilisb 12.5 17 30 100 100 1 1 1 Ficke et al. 2012 P. gracilisb 23 17 30 100 100 1 1 1 Ficke et al. 2012 Pseudorasbora parvac 12 3 2202135þ 85 1 1 1 Stakenas et al. 2009 P. parvac 12 3 2 20 20 0 1 1 1 Stakenas et al. 2009 P. parvac 12 3 2202065þ 95 1 2 1 Stakenas et al. 2009 Pylodictis olivarise 8.5 3 2.1 72 300 100 92 2 2 2 Daugherty and Buckmeier 2009 P. olivarise 8.5 3 2.1 72 300 98 91.67 2 4 2 Daugherty and Buckmeier 2009 Rutilus rutilus 12 3 2.1 J 80 182 100 100 1 1 1 Bolland et al. 2009 R. rutilusb 23 3 3.4 J 80 182 99 98 1 1 1 Bolland et al. 2009 Sander vitreus 12 930 1,461 98 2 6 3 Vandergoot et al. 2012 Scaphirhyncus albus 12 J 40 189 85 100 2 2 1 Hamel et al. 2013 S. albus 12 J 40 189 83 100 2 4 1 Hamel et al. 2013 Semotilus atromaculatusb 12.5 19 30 95 68 1 1 1 Ficke et al. 2012 S. atromaculatusb 23 16 30 100 63 1 1 1 Ficke et al. 2012 Silurus glanis 12 3 2.2 5 15 100 100 1 1 1 Rees et al. 2014 S. glanisa 12 3 2.2 5 15 100 100 1 1 1 Rees et al. 2014 S. glanis 12 3 2.2 65 455 85 1 1 2 Rees et al. 2014 a Fish were also tagged with another type of tag (T-bar anchor, opercular, etc.). b Sutures were used to close wounds. c All mortalities could be attributed to an unrelated outbreak of fungal infection. d Plastic infusion process PIT tags were used. e Each Fish in this study had two PIT tags in different locations. ..Msemne al. et Musselman W.C. PIT Tag Retention and Survival W.C. Musselman et al.

Table 3. Survival (S) and passive integrated transponder (PIT) tag retention (R) of six warmwater fish species that were collected from Flint Creek, Oklahoma, in 2012 to determine PIT tag retention in the laboratory. The six species included in the study were Cardinal Shiner Luxilus cardinalis, Central Stoneroller Campostoma annomalum, Slender Madtom Noturus exilis, Orangethroat Darter Etheostoma spectabile, Greenside Darter Etheostoma blennioides, and Smallmouth Bass Micropterus dolomieu. All fish were tagged in the peritoneum using 12- or 23-mm (tag size) half duplex PIT tags. Survival and PIT tag retention were reported after 30, 60, and 90 d. Survival was reported cumulatively across all time steps, whereas retention was reported as the number of living fish that retained their tags at each time step. We reported the number of fish (N) on occasions where survival or retention was not 100%. Growth (G, weightfinal weightinitial) was represented as positive (þ) or negative () after 30 d. We reported the test statistic resulting from Welch’s t-test where comparisons were made between growth of treatment and control groups (differences between groups).

30 d 60 d 90 d Common name N S (%) R (%) S (%) R (%) S (%) R (%) G Differences between groups

Cardinal Shiner 12 100 100 100 100 100 100 þ t18.60 ¼0.35, P ¼ 0.73, r ¼ 0.08 Central Stoneroller 8 100 100 88 (7/8) 100 88 (7/8) 100 þ t9.96 ¼ 0.29, P ¼ 0.78, r ¼ 0.09 a Slender Madtom 13 100 100 100 100 NA NA t21.87 ¼ 1.21, P ¼ 0.24, r ¼ 0.25 Orangethroat Darter 9 89 (8/9) 88 56 80 (4/5) NA NA t13.42 ¼ 1.41, P ¼ 0.18, r ¼ 0.36 Greenside Darter 3 100 100 100 100 NA NA t2.33 ¼ 0.18, P ¼ 0.87, r ¼ 0.12 Smallmouth Bass 25 96 100 96 100 NA NA þ t4.26 ¼0.41, P ¼ 0.70, r ¼ 0.20 a NA ¼ not applicable. analysis suggests that for studies that last up to 60 d, the mon in our review, with the vast majority showing no use of intracoelomic PIT tags to monitor the population difference. Whereas we did not explicitly test different of our six species is a viable approach. Above that 60-d methods of implanting the PIT tag, the use of a window, PIT tag retention in other species has shown to hypodermic needle did not affect our study species. consistently be greater than 90% (e.g., Alligator Gar This is in contrast to Baras et al. (1999) who found higher Atractosteus spatula, Longnose Gar Lepisosteus osseus, mortality in Nile Tilapia injected with PIT tags and Spotted Gar Lepisosteus oculatus, Largemouth Bass; suggested that this was attributable to their difficulty Buckmeier and Reeves 2012; Siepker et al. 2012), controlling penetration of the syringe. Given the high suggesting use in long-term experiments may be survival and retention rate, placing the PIT tag in the appropriate. A field-based study of adult Muskellunge peritoneal cavity seems appropriate for the species we Esox masquinongy using a combination PIT and T-bar studied. Other tagging locations or tag designs may anchor tags found that even up to 10 y post tagging, the need to be considered for applications where concerns probability of PIT tag loss was less than 1% (Rude et al. exist about the tags being potentially consumed by 2011). For our study, injection (implantation via incision humans (e.g., Daugherty and Buckmeier 2009; Siepker et in the Smallmouth Bass) into the peritoneal resulted in al. 2012). high tag retention; however, anatomical location and We found no reduction in growth related to the implantation method can highly influence that parame- tagging procedure across any of our study species. ter. For example, for Topmouth Gudgeon Pseudorasbora However, weight loss was apparent in both control and parva tag loss was much lower in individuals tagged in treatment groups for three of our species: Slender the flank (35%) compared to those implanted in the Madtom, Orangethroat Darter, and Greenside Darter. ventral area (65%; Stakenas et al. 2009). Conversely, a Similarly, our review suggested weight loss in treatment laboratory study of Shorthead Sculpin Cottus confusus fish was generally matched by growth rates of control found significantly higher retention in tags implanted in fish (e.g., Gardunio and Myrick 2012). Several studies, the body cavity (95 6 5.06%) compared to those located however, have highlighted an immediate post tagging in base of the spinous dorsal fin (23.75 6 11.39%; reduction in growth, which is later compensated by an Zaroban and Anglea 2010). Tagging method can also increased growth rate (e.g., Baras et al. 1999; Ruetz et al. partly determine retention. Baras et al. (1999) found use 2006). This initial growth slowdown has been linked to of sutures reduced short-term tag expulsion (and potential ‘‘compression of the digestive system’’ (Navarro protrusion of viscera) in Nile Tilapia Oreochromis niloticus. et al. 2006). It is also possible that growth reductions may With the exception of Orangethroat Darter, we found relate to a response by some wild fish to being held in survival to 60 d was high (88%). Our finding agrees captivity. with the results of the review where median survival of The results of our retention and survival trials were the 97 experiments was 92%. Lower survival in Orange- largely consistent with data obtained from the literature throat Darter may have been due to diet as weight loss review. Whereas the studies included in our review are was observed in both treatment and control fish. This is by no means exhaustive (i.e., there are numerous in line with the finding of other studies where higher available databases), by undertaking the literature search mortalities of PIT tagged fish were potentially driven by in a systematic manner, we aimed to reduce bias in study external factors rather than the procedure itself (e.g., selection. Despite the limitations in the literature pool disease, Castro-Santos and Vono 2013; overwinter (e.g., specificity of search terms and absence of gray mortality, Rees et al. 2014). Significant differences in literature; see Pullin and Stewart 2006), we believe the survival between tagged and control fish were uncom- review highlights some important overall trends. First,

Journal of Fish and Wildlife Management | www.fwspubs.org December 2017 | Volume 8 | Issue 2 | 360 PIT Tag Retention and Survival W.C. Musselman et al.

tested. Second, although most studies determined the effect of PIT tag use on a combination of tag retention, fish survival or growth, fewer studies have assessed the effect of tag use on fish behavior (but see Knaepkens et al. 2007; Ficke et al. 2012). Third, there is a dearth of information from outside North America and Europe, a phenomenon that has been identified in other areas of ecology (e.g., Wilson et al. 2007; Pysekˇ et al. 2008; Archer et al. 2014). Given the applications of PIT tags to the conservation and management of fish species, information on a broader range of species from across a wider range of geographic locations would be beneficial. It is also important to recognize that the skill level of persons tagging fish could also affect tag retention and survival and thus warrants consideration. Lastly, examining possible behavioral changes associated with tagging could broaden the use of PIT tagging, especially in small- bodied fishes. Overall, the specific attributes of tagging studies are related to tagging objectives (e.g., survival, growth, and behavior), but reporting information on study duration, weight and length of tagged fish, handling and injection procedures, and use of control fish would benefit a more comprehensive examination of tag effects.

Supplemental Material

Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any Figure 1. Initial mean weight (white bar, 695% confidence supplemental material. Queries should be directed to the limits) and weight after 30 d (gray bars, 695% confidence corresponding author for the article. limits) of six warmwater fish species that were collected from Flint Creek, Oklahoma, in 2012 to determine passive integrated Table S1. Spreadsheet containing three tables. Table 1 transponder (PIT) tag retention in the laboratory. All treatment is a description of field headings used in Tables 2 and 3. fish were tagged in the peritoneum with 12- or 23-mm (tag Data described are from a laboratory study of passive size) half duplex PIT tags. Control fish were handled in the same integrated transponder (PIT) tag retention and survival of manner as treatment fish, but no tagging occurred. Weight was six warmwater fish species (scientific names provided in not significantly different between PIT tag treatment and parentheses) that were collected from Flint Creek, control groups for all species (a ¼ Cardinal Shiner Luxilus Oklahoma, in 2012. All fishes were tagged in the cardinalis;b¼ Central Stoneroller Campostoma annomalum;c¼ peritoneum with 12- or 23-mm (tag size) half duplex Slender Madtom Noturus exilis;d¼ Orangethroat Darter PIT tags. Table 2 provides data on the total length (mm) Etheostoma spectabile;e Greenside Darter Etheostoma ¼ and relative growth (g, difference in weight from the blennioides;f¼ Smallmouth Bass Micropterus dolomieu). beginning to end of trials) of treatment (trt) and control (c) fishes (OTD ¼ Orangethroat Darter Etheostoma PIT tag retention and survival of tagged fishes were spectabile; GRN ¼ Greenside Darter Etheostoma blen- generally high; however, examples of high tag loss (e.g., nioides; SLND ¼ Slender Madtom Noturus exilis; CARD ¼ Stakenas et al. 2009; Zaroban and Anglea 2010) and Cardinal Shiner Luxilus cardinalis; CSTN ¼ Central Stone- elevated mortality (e.g., Orangethroat Darter, this study; roller Campostoma annomalum; and SMB ¼ Smallmouth Ficke et al. 2012) were apparent. This is consistent with Bass Micropterus dolomieu). The treatment group was Rees et al. (2014) who suggested the ‘‘tagging efficiency subjected to intracoelomic-placed 12- or 23-mm (tag is largely context-dependent’’ and therefore comparison size) half duplex passive integrated transponder tags. across species and methods should be treated with The 23-mm tags were only used to tag Smallmouth Bass caution (Archdeacon et al. 2009). Survival and retention due to their larger size at tagging. Control fishes were seem to be a function of a multitude of variables subject to the same handling as treatment fishes (i.e., including species (e.g., Stakenas et al. 2009; Ficke et al. anesthetized, measured, and weighed), but they were 2012), tagging location (e.g., Zaroban and Anglea 2010), not tagged. The same person (W.C.M.) conducted all and tagging methodology (e.g., Archdeacon et al. 2009). tagging in the laboratory in 2012. Table 3 provides data Therefore, it would seem prudent to examine the effect on the total length (mm) and survival (30, 60, and 90 d) of PIT tag use under controlled conditions before of treatment (trt) and control (c) fishes (OTD ¼ Orange- applying alternative tagging methodologies or to new throat Darter Etheostoma spectabile; GRN ¼ Greenside species in situations where the assumptions cannot be Darter Etheostoma blennioides; SLND ¼ Slender Madtom

Journal of Fish and Wildlife Management | www.fwspubs.org December 2017 | Volume 8 | Issue 2 | 361 PIT Tag Retention and Survival W.C. Musselman et al.

Noturus exilis; CARD ¼ Cardinal Shiner Luxilus cardinalis; Bodine KA, Fleming P. 2014. Retention of PIT and T-bar CSTN ¼ Central Stoneroller Campostoma annomalum; anchor tags in Blue Catfish. North American Journal of and SMB ¼ Smallmouth Bass Micropterus dolomieu). The Fisheries Management 34:68–71. doi: 10.1080/ treatment group was subjected to intracoelomic-placed 02755947.2013.860064 12- or 23-mm (tag size) half duplex passive integrated Bolland JD, Cowx IG, Lucas MC. 2009. Evaluation of VIE transponder tags. The 23-mm tags were only used to tag and PIT tagging methods for juvenile cyprinid fishes. Smallmouth Bass due to their larger size at tagging. Journal of Applied Ichthyology 25:381–386. doi: 10. Control fishes were subject to the same handling as 1111/j.1439 0426.2009.01261.x treatment fishes (i.e., anesthetized, measured, and weighed), but they were not tagged. The number of Bonar SA, Hubert WA, Willis DW. 2009. Standard methods fishes surviving is provided if less than 100%. for sampling North American freshwater fishes. Found at DOI: http://dx.doi.org/10.3996/122016- Bethesda, Maryland: American Fisheries Society. JFWM-091.S1 (20 KB XLSX). Buckmeier DL, Reeves KS. 2012. Retention of passive integrated transponder, T-bar anchor, and coded wire Acknowledgments tags in lepisosteids. North American Journal of Fisheries Management 32:573–576. doi: 10.1080/ This research is a contribution of the Oklahoma 02755947.2012.678968 Cooperative Fish and Wildlife Research Unit (U.S. Burdick SM. 2011. Tag loss and short-term mortality Geological Survey, Oklahoma Department of Wildlife associated with passive integrated transponder tag- Conservation, Oklahoma State University, and Wildlife ging of juvenile Lost River Suckers. North American Management Institute cooperating). Funding was pro- Journal of Fisheries Management 31:1088–1092. doi: vided by the Oklahoma Department of Wildlife Conser- 10.1080/02755947.2011.641067 vation. This study was performed under the auspices of Burnham KP, Anderson DR, White GC, Brownie C, Pollock Oklahoma State University animal use protocol AG1110. KH. 1987. Design and analysis methods for fish survival We thank C. Kemp for providing laboratory assistance. experiments based on release–recapture. Bethesda, We thank the Associate Editor and three anonymous Maryland: American Fisheries Society Monographs 5. reviewers for their recommended improvements to the Castro-Santos T, Vono V. 2013. Posthandling survival and manuscript. PIT tag retention by Alewives – a comparison of Any use of trade, product, website, or firm names in gastric and surgical implants. 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